Deep-sea Ecosystem Functioning Research Articles

Habitat heterogeneity effects on microbial communities of the Gulf of Maine

Many biological and physical variables influence microbes at the sediment-water interface, whose response to those variables affects the overall fate and residence time of organic matter (OM) in the marine environment. In addition to the many ecological roles microbes play in deep-sea sediments, further studies are needed to address microbial community diversity and its influence on seafloor organic matter remineralization rates. We explored microbial diversity, distribution, and associated organic matter remineralization among contrasting habitats and following 24-h experimental phytodetrital enrichment of sediments from Canyon, Inter-Canyon, and Channel habitats of the Gulf of Maine, Northwest Atlantic. Based on multivariate analyses of community composition we found that habitat heterogeneity influenced microbial community composition but not microbial diversity. Similarly, the phytodetrital addition did not translate to significant differences in microbial diversity but altered nitrate flux in Inter-canyon sediments and phosphate flux in Channel sediments. Bacteria were dominant over Archaea and, of the environmental variables we measured, quantity and quality of organic matter best explained overall microbial community variation. Proteobacteria, Bacteroidae, Acidobacteriota, Planctomycetota, and NB1-J Deltaproteobacteria dominated all habitats, but variation in the microbial community at our study sites explained only 7% of nutrient fluxes. Our exploratory study did not suggest a strong contribution of microbial community composition to OM remineralization variation both among contrasting habitats and in response to phytodetrital addition, and thus to this aspect of deep-sea ecosystem functioning, at least over short-term incubations.

Combined use of carbon, nitrogen and sulfur stable isotopes reveal trophic structure and connections in deep-sea mesopelagic and demersal fish communities from the Southeastern Pacific Ocean

The trophic structure of deep-sea fish communities has been poorly studied in the Southeastern Pacific Ocean. Here, using the analysis of multiple (CNS) stable isotopes, we provide a first approach to characterize the structure of a marine food web including mesopelagic (9 species) and demersal (13 species) fishes. At a species level, Dissostichus eleginoides were the most 13C-depleted and the grenadier Coryphaenoides ariommus the most 13C-enriched species. The most 15N-depleted species was the lanternfish Diogenichthys laternatus and macrourid fishes Trachyrincus villagai and C. ariommus the most 15N-enriched. δ34S values showed less variation, but ranged considerably, varying between 10.5 and 17.7‰: C. ariommus was the most 34S-depleted species and D. eleginoides the most 34S-enriched. At a whole study level, individual δ13C and δ15N values were positively correlated. Relationships between δ13C and δ34S, and δ15N and δ34S were both negative. When analyses were conducted separately for demersal and mesopelagic fishes, δ13C showed a positive correlation with δ15N. There was a negative relationship between δ13C and δ34S in demersal fish but no apparent relationship between δ15N and δ34S. In mesopelagic fishes, there was no statistical support for relationships between δ13C and δ34S or δ15N and δ34S. Mean log-transformed total length (TL) and mean δ15N were related in mesopelagic fishes, but there was no apparent relationship between TL and δ13C or δ34S values. In the case of demersal fishes there was no relationship between TL and either δ15N, δ13C or δ34S. Using cluster analysis, species were classified into 4 distinct trophic groups (G1 - G4) that display different trophic strategies according to the literature. Groups G1 and G2 included zooplanktivorous, micronektonivorous and gelatinovorous fishes associated with pelagic habitats. Groups G3 and G4 include micronektonivorous, piscivorous and generalist fishes foraging in benthic habitats. The demersal fish Dissostichus eleginoides was classified as a member of G1, suggesting that its diet in northern Chile is likely dominated by pelagic prey. In addition, Macrourus holotrachys (G3) showed very marked individual variability in δ15N values indicating considerable intraspecific variation in diet and foraging behavior. Given that this species had isotope values that extended across values typical of benthic and pelagic habitats, it suggests that some individuals may perform vertical migrations. Our results also highlighted that some demersal species (M. holotrachys and Coryphaenoides ariommus) had δ34S values that indicate the assimilation of some chemosynthetic-derived sulfur.Our results provide isotopic information on deep-water species in this region and show likely coupling between the demersal and mesopelagic assemblages. This information improves our understanding of deep-sea ecosystem functioning and provides key information for fisheries management and conservation initiatives.

Three new deep-sea species of Thyasiridae (Mollusca: Bivalvia) from the northwestern Pacific Ocean

The Thyasiridae is one of the species-richest families in the abyssal and hadal zones of the northwestern Pacific Ocean. Many thyasirid species dominate benthic communities in terms of abundance and play an important role in the functioning of deep-sea ecosystems. Most of the thyasirid species in the region are new to science and have not been described. Based on the material collected from 1954 to 2016 by seven deep-sea expeditions, three new species of Thyasiridae (Parathyasira coani sp. nov., P. pauli sp. nov., and Thyasira kharkovensis sp. nov.) are described from the abyssal and hadal zones (3210–7540 m depth) of the Sea of Okhotsk, the Bering Sea, as well as the Kuril-Kamchatka and Japan trenches. The new species are remarkable among their congeners due to the combination of the following characters: an obliquely-rhomboidal shell with a weak and shallow posterior sulcus and a large prodissoconch with sculpture of lamellated folds. Comparisons with related species are provided.

Benthic megafauna of the western Clarion-Clipperton Zone, Pacific Ocean.

There is a growing interest in the exploitation of deep-sea mineral deposits, particularly on the abyssal seafloor of the central Pacific Clarion-Clipperton Zone (CCZ), which is rich in polymetallic nodules. In order to effectively manage potential exploitation activities, a thorough understanding of the biodiversity, community structure, species ranges, connectivity, and ecosystem functions across a range of scales is needed. The benthic megafauna plays an important role in the functioning of deep-sea ecosystems and represents an important component of the biodiversity. While megafaunal surveys using video and still images have provided insight into CCZ biodiversity, the collection of faunal samples is needed to confirm species identifications to accurately estimate species richness and species ranges, but faunal collections are very rarely carried out. Using a Remotely Operated Vehicle, 55 specimens of benthic megafauna were collected from seamounts and abyssal plains in three Areas of Particular Environmental Interest (APEI 1, APEI 4, and APEI 7) at 3100-5100 m depth in the western CCZ. Using both morphological and molecular evidence, 48 different morphotypes belonging to five phyla were found, only nine referrable to known species, and 39 species potentially new to science. This work highlights the need for detailed taxonomic studies incorporating genetic data, not only within the CCZ, but in other bathyal, abyssal, and hadal regions, as representative genetic reference libraries that could facilitate the generation of species inventories.

Particle fluxes in submarine canyons along a sediment-starved continental margin and in the adjacent open slope and basin in the SW Mediterranean Sea

Investigating the transfer of particulate matter from the continental shelf to the deep basin is critical to understand the functioning of deep sea ecosystems. In this paper we present novel results on the temporal variability of particle fluxes to the deep in three physiographic domains of a 240 km long margin segment and nearby basin off Murcia and Almeria provinces in the SW Mediterranean Sea, which are submarine canyons forming a rather diverse set (namely Escombreras, Garrucha-Almanzora and Almeria), the adjacent open slope and the deep basin.This margin is located off one of the driest regions in Europe and, therefore, its study may help understanding how mainland aridity translates into the export of particles to deep margin environments. Five mooring lines equipped with currentmeters, turbidity-meters and sediment traps were deployed for one entire annual cycle, from March 2015 to March 2016. We combine oceanographic, hydrological and meteorological data with grain size and bulk elemental data (organic carbon, opal, CaCO3, lithogenic) from the collected sinking particles to understand what drives particle transfers in such an under-studied setting, and to quantify the resulting fluxes and assess their spatio-temporal variability.Weighted total mass fluxes in canyons range from 1.64 g m−2 d−1 in Almeria Canyon to 7.33 g m−2 d−1 in Garrucha-Almanzora Canyon system, which are rather low values compared to other submarine canyons in the Western Mediterranean Sea. This results from the absence of extreme wind-storm events during the investigated time period combined with the reduced sediment input to the inner shelf by river systems in the study area. Our results also show that wind-storms are the main trigger for off-shelf particle transport to the deep margin, both within submarine canyons and over the open slope. The most significant transfer period is associated to a set of north-eastern storms in early spring 2015, when the off-shelf transport likely was promoted by storm-induced downwelling. However, the prevailing oceanographic conditions restricts the advection of water down the canyon heads to a few hundred meters, thus promoting a bottom-detached transport of particles seaward. Overall physiography, canyon head incision into the continental shelf and the distance of the canyon head to the shoreline (e.g. very short in Garrucha Canyon) play a key role in particle trapping capability and, therefore, in easing downslope particle transport. Further, bottom trawling activities around the Garrucha-Almanzora Canyon system, feed a nepheloid layer at depths in excess of 400 m, subsequently enhancing particle fluxes throughout the study period. In contrast, maximum particle fluxes in the deep basin respond to seasonal phytoplankton blooms.Our study shows that particle export from the shallow inner margin to the deep outer margin in sediment-starved settings, even if limited, does occur as dominated by atmosphere and ocean driven short-lived events. However, that export does not reach too far as at several tens of kilometres from the shelf edge advective fluxes are replaced by vertical ones impelled by phytoplankton dynamics.

Functional Pattern of Benthic Epifauna in the Chukchi Borderland, Arctic Deep Sea

Assessment of Arctic deep-sea ecosystem functioning is currently an urgent task considering that ongoing sea-ice reduction opens opportunities for resource exploitation of yet understudied deep-sea regions. We used Biological Trait Analysis to evaluate ecosystem functioning and test if common paradigms for deep-sea fauna apply to benthic epifauna of the deep-sea Arctic Chukchi Borderland (CBL). We also investigated the influence of environmental factors on the functional structure of the epifauna. The analysis was performed for 106 taxa collected with a beam trawl and a Remotely Operated Vehicle from 486 to 2610 m depth. The most common trait modalities were small-medium size, mobile, benthic direct and lecithotrophic larval development, and predatory feeding, which mostly supports the current view of epifauna in the global deep sea. Functional composition of epifauna differed between two depth strata (486–1059 m and 1882–2610 m), with depth and sediment carbon content explaining most of the functional variability. Proportional abundances of the modalities free-living, swimming, suspension feeders, opportunists/scavengers, internal fertilization and globulose were higher at deep stations. Functional redundancy (FR) was also higher there compared to the mid-depth stations, suggesting adaptation of fauna to the more homogeneous deep environment by fewer and shared traits. Mid-depth stations represented higher functional variability in terms of both trait modality composition and functional diversity, indicating more variable resource use in the more heterogeneous habitat. Food input correlated positively with the proportional abundance of the modalities tube-dwelling, sessile and deposit feeding. Areas with drop stones were associated with higher proportional abundance of the modalities attached, upright, and predators. Comparatively low FR may render the heterogeneous mid-depth area of the CBL vulnerable to disturbance through the risk of loss of functions. Across the study area, high occurrence of taxa with low dispersal ability among adult and larval life stages may prevent rapid adaptation to changes, reduce ability to recolonize and escape perturbation.

The deep sea: The new frontier for ecological restoration

Deep-sea ecosystems are the most extensive on Earth and provide key goods and services for human well-being, such as genetic resources and climate regulation. Maintaining the sustainable functioning of the global biosphere therefore requires protection of deep-sea ecosystems, particularly because these ecosystems face major changes related to human and climate-induced impacts. Although we lack data to evaluate the spatial scale of degraded deep-sea habitats, numerous studies document human impacts on the whole ocean. However, protection alone can be insufficient to reverse habitat degradation in the deep sea. Scientifically, deep-sea restoration actions may be feasible, but whether such actions will achieve sustainability goals when applied at broad spatial scales of impact remain questionable. Successful application of most restoration efforts will first require a deeper understanding of biodiversity and functioning of deep-sea ecosystems, and better knowledge of ecosystem resilience and recovery rates of deep-sea fauna. In addition to limited data availability, expensive technologies (with estimated costs up to millions of dollars ha−1) represent a major obstacle to large-scale deep-sea restoration, but international cooperation (like a stronger collaboration between industry and scientists belonging to the academia) could significantly reduce this operational cost. Future deep-sea ecosystem restoration could offer an important business opportunity for technological development and application and an investment in natural capital for a new and competitive blue-growth sector.

High diversity of benthic bacterial and archaeal assemblages in deep-Mediterranean canyons and adjacent slopes

Submarine canyons and slopes increase the topographic heterogeneity of continental margins and enhance mass and energy transfer from the shelf to the deeper basins, profoundly influencing the biodiversity and functioning of deep-sea ecosystems. However, information on the distribution and diversity of microbial assemblages in such habitats is extremely scant. In the present study, for the first time, we investigated abundances of benthic prokaryotes and their diversity (i.e., bacterial and archaeal) in two of the largest canyons of the Mediterranean Sea (Bisagno and Polcevera Canyons, in the Ligurian Margin) and their adjacent open slope along a water-depth gradient from 200 to 2000 m. We found that prokaryotic abundance and the richness of Operational Taxonomic Units (OTUs) varied within a narrow range despite the high variability of thermohaline and trophic conditions in the habitats investigated. Conversely, the taxonomic composition (in terms of OTUs) was highly variable among the different habitats and depths investigated. The largest fraction of OTUs (representing >80% of the total OTUs identified) were unique of each sampling site, indicating a high prokaryotic β-diversity among the investigated systems. Thermo-haline and trophic conditions and water depth only partially influenced the composition of the prokaryotic assemblages suggesting that other factors, potentially related to physical forcing typically occurring in margin ecosystems, could promote a high diversification of benthic bacterial and archaeal assemblages. This study provides new insights into the benthic prokaryotic diversity of Ligurian canyons and suggests that microbial assemblages thriving in continental margins can largely contribute to the whole diversity of Mediterranean deep-sea ecosystems.

Virus decomposition provides an important contribution to benthic deep-sea ecosystem functioning

Viruses are key biological agents of prokaryotic mortality in the world oceans, particularly in deep-sea ecosystems where nearly all of the prokaryotic C production is transformed into organic detritus. However, the extent to which the decomposition of viral particles (i.e., organic material of viral origin) influences the functioning of benthic deep-sea ecosystems remains completely unknown. Here, using various independent approaches, we show that in deep-sea sediments an important fraction of viruses, once they are released by cell lysis, undergo fast decomposition. Virus decomposition rates in deep-sea sediments are high even at abyssal depths and are controlled primarily by the extracellular enzymatic activities that hydrolyze the proteins of the viral capsids. We estimate that on a global scale the decomposition of benthic viruses releases ∼37-50 megatons of C per year and thus represents an important source of labile organic compounds in deep-sea ecosystems. Organic material released from decomposed viruses is equivalent to 3 ± 1%, 6 ± 2%, and 12 ± 3% of the input of photosynthetically produced C, N, and P supplied through particles sinking to bathyal/abyssal sediments. Our data indicate that the decomposition of viruses provides an important, previously ignored contribution to deep-sea ecosystem functioning and has an important role in nutrient cycling within the largest ecosystem of the biosphere.

Evolutionary origins of hydrothermal vents metazoans

The discovery of the oases associated with hydrothermal vents in the deep sea, is probably the most fascinating discovery of oceanography of the last century. In this habitat, contrary to all expectations, a thriving development of unknown organisms was observed. At that time the knowledge about the deep sea organisms was very scarce and the accepted hypotheses about their evolutionary origins, their physiology or their ecology were very speculative. Almost forty years later, exploration of the deep-sea realm, but also of paleontological data together with the improvements in the phylogenetic methods, allowed the rejection of the hypothesis of an evolutionary history cut off the rest of the marine realm. 1. Life in the deep sea: Knowledge is recent Inthe thirtyyears after the discovery of the deep-sea oases associated with hot vents much of the research efforts of the marine biologists have been devoted to this exceptional environment and its inhabitants. However, when the hot vents have been discovered, the deep-sea realm was still poorly known. At this time, most of the available hypotheses about the functioning of deep sea ecosystems, or about the physiology or the evolutionary origins of the organisms were very speculative. In this historical context, I selected three hypotheses which I feel have played a major role in the analysis of the diversity of hot vents' organisms and their evolutionary origins.

Bioavailability of sinking organic matter in the Blanes canyon and the adjacent open slope (NW Mediterranean Sea)

Abstract. Submarine canyons are sites of intense energy and material exchange between the shelf and the deep adjacent basins. To test the hypothesis that active submarine canyons represent preferential conduits of available food for the deep-sea benthos, two mooring lines were deployed at 1200 m depth from November 2008 to November 2009 inside the Blanes canyon and on the adjacent open slope (Catalan Margin, NW Mediterranean Sea). We investigated the fluxes, biochemical composition and food quality of sinking organic carbon (OC). OC fluxes in the canyon and the open slope varied among sampling periods, though not consistently in the two sites. In particular, while in the open slope the highest OC fluxes were observed in August 2009, in the canyon the highest OC fluxes occurred in April–May 2009. For almost the entire study period, the OC fluxes in the canyon were significantly higher than those in the open slope, whereas OC contents of sinking particles collected in the open slope were consistently higher than those in the canyon. This result confirms that submarine canyons are effective conveyors of OC to the deep sea. Particles transferred to the deep sea floor through the canyons are predominantly of inorganic origin, significantly higher than that reaching the open slope at a similar water depth. Using multivariate statistical tests, two major clusters of sampling periods were identified: one in the canyon that grouped trap samples collected in December 2008, concurrently with the occurrence of a major storm at the sea surface, and associated with increased fluxes of nutritionally available particles from the upper shelf. Another cluster grouped samples from both the canyon and the open slope collected in March 2009, concurrently with the occurrence of the seasonal phytoplankton bloom at the sea surface, and associated with increased fluxes of total phytopigments. Our results confirm the key ecological role of submarine canyons for the functioning of deep-sea ecosystems, and highlight the importance of canyons in linking episodic storms and primary production occurring at the sea surface to the deep sea floor.

Unravelling the environmental drivers of deep-sea nematode biodiversity and its relation with carbon mineralisation along a longitudinal primary productivity gradient

Abstract. Alongside a primary productivity gradient between the Galicia Bank region in the Northeast Atlantic and the more oligotrophic eastern Mediterranean Basin, we investigated the bathymetric (1200–3000 m) and longitudinal variation in several measures for nematode taxon (Shannon–Wiener genus diversity, expected genus richness and generic evenness) and functional diversity (trophic diversity, diversity of life history strategies, biomass diversity and phylogenetic diversity). Our goals were to establish the form of the relation between diversity and productivity (measured as seafloor particulate organic carbon or POC flux), and to verify the positive and negative effect of sediment particle size diversity (SED) and the seasonality in POC flux (SVI), respectively, on diversity, as observed for other oceanographic regions and taxa. In addition, we hypothesised that higher taxon diversity is associated with higher functional diversity, which in turn stimulates nematode carbon mineralisation rates (determined from biomass-dependent respiration estimates). Taxon diversity related positively to seafloor POC flux. Phylogenetic diversity (measured as average taxonomic distinctness) was affected negatively by the magnitude and variability in POC flux, and positively by SED. The latter also showed an inverse relation with trophic diversity. Accounting for differences in total biomass between samples, we observed a positive linear relation between taxon diversity and carbon mineralisation in nematode communities. We could, however, not identify the potential mechanism through which taxon diversity may promote this ecosystem function since none of the functional diversity indices related to both diversity and nematode respiration. The present results suggest potential effects of climate change on deep-sea ecosystem functioning, but further also emphasise the need for a better understanding of nematode functions and their response to evolutionary processes.

Deep-sea echinoderm oxygen consumption rates and an interclass comparison of metabolic rates in Asteroidea, Crinoidea, Echinoidea, Holothuroidea and Ophiuroidea

Echinoderms are important components of deep-sea communities because of their abundance and the fact that their activities contribute to carbon cycling. Estimating the echinoderm contribution to food webs and carbon cycling is important to our understanding of the functioning of the deep-sea environment and how this may alter in the future as climatic changes take place. Metabolic rate data from deep-sea echinoderm species are, however, scarce. To obtain such data from abyssal echinoderms, a novel in situ respirometer system, the benthic incubation chamber system (BICS), was deployed by remotely operated vehicle (ROV) at depths ranging from 2200 to 3600 m. Oxygen consumption rates were obtained in situ from four species of abyssal echinoderm (Ophiuroidea and Holothuroidea). The design and operation of two versions of BICS are presented here, together with the in situ respirometry measurements. These results were then incorporated into a larger echinoderm metabolic rate data set, which included the metabolic rates of 84 echinoderm species from all five classes (Asteroidea, Crinoidea, Echinoidea, Holothuroidea and Ophiuroidea). The allometric scaling relationships between metabolic rate and body mass derived in this study for each echinoderm class were found to vary. Analysis of the data set indicated no change in echinoderm metabolic rate with depth (by class or phylum). The allometric scaling relationships presented here provide updated information for mass-dependent deep-sea echinoderm metabolic rate for use in ecosystem models, which will contribute to the study of both shallow water and deep-sea ecosystem functioning and biogeochemistry.

Ecosystem effects of dense water formation on deep Mediterranean Sea ecosystems: an overview

Natural episodic events, such as gravity flows, submarine landslides, and benthic storms can determine severe modifications in the structure and functioning of deep-sea ecosystems. Here, we report and compare the ecosystem effects produced by dense water formation events that occurred in the Gulf of Lions (NW Mediterranean) and the Aegean Sea (NE Mediterranean). In both regions, the rapid sinking of cold dense waters, driven by regional meteorological forcings, results in important immediate modifications that can be summarised in: (i) increased organic matter content in the deep basin; (ii) diminished benthic abundance; and (iii) changes of benthic biodiversity. At longer time scale the analysis reveals, however, different resilience times in the two regions. The Gulf of Lions is characterized by a very fast (months) recovery whereas the Aegean Sea shows much longer (45 years) resilience time. New long-term studies are further needed to identify the potential effects that changes in the duration, intensity and frequency of episodic events could have on the structure, biodiversity and functioning of the deep Mediterranean Sea under environmental and climate change scenarios.

Ecosystem effects of dense water formation on deep Mediterranean Sea ecosystems: an overview

Natural episodic events, such as gravity flows, submarine landslides, and benthic storms can determine severe modifications in the structure and functioning of deep-sea ecosystems. Here, we report and compare the ecosystem effects produced by dense water formation events that occurred in the Gulf of Lions (NW Mediterranean) and the Aegean Sea (NE Mediterranean). In both regions, the rapid sinking of cold dense waters, driven by regional meteorological forcings, results in important immediate modifications that can be summarised in: (i) increased organic matter content in the deep basin; (ii) diminished benthic abundance; and (iii) changes of benthic biodiversity. At longer time scale the analysis reveals, however, different resilience times in the two regions. The Gulf of Lions is characterized by a very fast (months) recovery whereas the Aegean Sea shows much longer (45 years) resilience time. New long-term studies are further needed to identify the potential effects that changes in the duration, intensity and frequency of episodic events could have on the structure, biodiversity and functioning of the deep Mediterranean Sea under environmental and climate change scenarios.

Exponential Decline of Deep-Sea Ecosystem Functioning Linked to Benthic Biodiversity Loss

Recent investigations suggest that biodiversity loss might impair the functioning and sustainability of ecosystems. Although deep-sea ecosystems are the most extensive on Earth, represent the largest reservoir of biomass, and host a large proportion of undiscovered biodiversity, the data needed to evaluate the consequences of biodiversity loss on the ocean floor are completely lacking. Here, we present a global-scale study based on 116 deep-sea sites that relates benthic biodiversity to several independent indicators of ecosystem functioning and efficiency. We show that deep-sea ecosystem functioning is exponentially related to deep-sea biodiversity and that ecosystem efficiency is also exponentially linked to functional biodiversity. These results suggest that a higher biodiversity supports higher rates of ecosystem processes and an increased efficiency with which these processes are performed. The exponential relationships presented here, being consistent across a wide range of deep-sea ecosystems, suggest that mutually positive functional interactions (ecological facilitation) can be common in the largest biome of our biosphere. Our results suggest that a biodiversity loss in deep-sea ecosystems might be associated with exponential reductions of their functions. Because the deep sea plays a key role in ecological and biogeochemical processes at a global scale, this study provides scientific evidence that the conservation of deep-sea biodiversity is a priority for a sustainable functioning of the worlds' oceans.